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Forum

Eco-Evolutionary sexual dimorphism (i.e., the trait differences Studies that correlate variation in ecologi-

between females and males; arrow 2 in cal conditions to population or species

Dynamics of Sexual

Figure 1B). Sexual dimorphism is ubiquitous variation in dimorphism are informative

Dimorphism in nature and encompasses a varietyoftraits but cannot distinguish ecological causes

that may impact communityandecosystem from effects of dimorphism (e.g., [7]).

1,2, ,@

David C. Fryxell , * dynamics. Given the recent interest in Thus, experimental manipulations are

2,@

Doriane E. Weiler, understanding community and ecosystem needed to test for community and eco-

3,@

effects of intraspecific trait variation in gen- system effects of sexual dimorphism.

Michael T. Kinnison, and

2,@ eral [4], the lack of empirical research on the Such direct tests have only recently

Eric P. Palkovacs

ecological consequences of sexual dimor- emerged (arrow 3, Figure 1B) and have

phism is surprising (arrow 3, Figure 1B). been performed at two levels of biological

Sexual dimorphism is widespread,

organization: the individual level and the

but we have a limited understand-

Evolved Sexual Dimorphism in population level.

ing of its significance for commu-

Ecological Roles

nities and ecosystems. Several

There has long been evidence of ecologi- The Extended Phenotype of

new experiments demonstrate that

cal dimorphism (i.e., sexual dimorphism in Dimorphism

sexual dimorphism can have far-

ecological roles). For example, the sexes Sex differences at the individual level can

reaching ecological effects. These commonly differ in diets in the field. These have community and ecosystem conse-

results suggest that sexual dimor- effects may be pronounced in cases of quences when communities assemble or

‘

phism and sexual selection are sexual size dimorphism, in which the ecosystems exist as extended pheno-

’

potent, but largely overlooked larger sex can feed on larger prey. In types of individual hosts (i.e., foundation

species without strong size dimorphism, species). For example, Nell and col-

components of eco-evolutionary

dynamics. ecological dimorphism may still be strong leagues [8] demonstrated that female

due to dimorphism in functional traits. For genotypes of the mulefat shrub (Baccha-

example, the sexes of the recently extinct ris salicifolia) had more flowers and grew

Eco-evolutionary dynamics describe huia (Heteralocha acutirostris), a New more quickly than did male genotypes

reciprocal effects between evolution and Zealand bird species that exhibited one cultivated in the same garden

population, community, and ecosystem of the most extreme cases of sexual (Figure 2C). This trait dimorphism led to

ecology. These dynamics can be broadly dimorphism in beak shape known, must dimorphism in hosted arthropod commu-

important when natural selection causes have fed on significantly different resour- nity composition; the more flower-laden

rapid trait changes to occur in a population, ces (Figure 2A) [5]. Another extreme eco- females had higher predator densities,

because the trait changes can have com- logical dimorphism is found in adult presumably because of increased visita-

munity- and ecosystem-wide consequen- mosquitoes: females feed on animal tion by nectar-feeding insect prey. Simi-

ces [1] (Figure 1A). There may also be blood, while males feed on plant nectar larly, Tsuji and Fukami [9] studied the

ecological consequences of evolutionary (e.g., Ochlerotatus sp., Figure 2B). microbe communities assembling on

responses to sexual selection. This male versus female flowers in the dioe-

hypothesis is primarily supported by theory Ecological dimorphism could be significant cious shrub Eurya emarginata (Figure 2D).

and experiments demonstrating that sex- even when sexual dimorphism is relatively Female flowers contained less nectar and

ual selection can affect population ecology inconspicuous. Forexample, thesexes may had significantly lower bacterial and fun-

[2] and by work showing that sexual selec- show little morphological dimorphism, but gal concentrations compared with male

tion can affect functional traits (i.e., those ecological dimorphism could arise from dif- flowers, apparently a result of differential

hypothesized to have community or eco- ferential habitat use [6]. More generally, it visitation by insects. Based on this and

system effects) [3]. However, the role of may be that most sexual organisms display related work, it may be that microbiomes

sexual selection in communities and eco- some degree of ecological dimorphism due are commonly forms of ‘extended sexual

systems remains largely untested. to divergent nutritional requirements dimorphism’ in plants and animals.

between the sexes, a product of differential

Selection has community and ecosystem reproductive investment. Even weak dimor- Studyingsexualdimorphismintheextended

consequences through its effects on traits phism could be important for communities phenotypes of foundation species provides

(Figure 1). Sexual selection can shape the and ecosystems in abundant or otherwise a clear-cut relationship between sexual

trait distribution of a population by affecting ecologically important populations. dimorphism and community and

Trends in Ecology & Evolution, Month Year, Vol. xx, No. yy 1

TREE 2534 No. of Pages 4

(A) (B)

Natura l Natural Sexual

sele con selecon selecon

Evoluon 1 2

Feedback

Popu laon

Nondimorphic Sexua l

fun conal trait 5 4

traits dimorph ism

distrib uon

E.g., species

interacons 3

Community and Commun ity and

ecosystem ecosyst em

ecology ecolo gy

Figure 1. The Conceptual Model. (A) The field of ‘eco-evolutionary dynamics’ has classically focused on the community and ecosystem effects of evolution by

natural selection (blue arrows) and has not focused on sexually dimorphic traits. The field has further aimed to parse feedbacks between evolution and ecology when

they act on similar timescales. (B) Recently, researchers have called for the explicit incorporation of sexual selection into this framework [2,3], which we expand in our

conceptual model to include two separate aspects of the trait distribution of a population: sexually dimorphic traits and nondimorphic traits. While both natural selection

(1) and sexual selection (2) affect sexual dimorphism (together, an effect referred to as ‘sex-specific selection’), to understand the link between sexual selection and

communities and ecosystems, we must understand the effect of sexual dimorphism on communities and ecosystems (3). Given that communities and ecosystems

shape sexual selection (4) and natural selection (5), future work could aim to parse eco-evolutionary feedbacks associated with sexual dimorphism.

ecosystem ecology. However, there is often seeks to compare differences in effects of ecological effects of mosquitofish are

interest in communities and ecosystems populations with trait distributions that are largely shaped by the sex ratio of popula-

assembling at larger spatial scales than more female or male biased. tions, which vary widely in nature.

those associated with individual hosts.

Moreover, from the eco-evolutionary Fryxell and colleagues [10] manipulated In the other sex ratio experiment, Start

dynamics perspective, the overarching goal population sex ratios of sexually dimorphic and De Lisle [11] manipulated sex ratios

is to test the ecological effects of evolution- mosquitofish (Gambusia affinis) in pond of predaceous newts (Notophthalmus vir-

ary change, which occurs in populations. mesocosms(Figure2E).Incontrasttomale idescens) in pond mesocosms

Thus, the unifying level of analysis for under- mosquitofish, females exhibit continuous (Figure 2F). While these newts do not

standing the effects of sexual dimorphism growth and have higher feeding and excre- show strong differences in feeding traits

on communities and ecosystems, and tion rates. In pond mesocosms, female- per se, the sexes differ substantially in

incorporating those effects into an eco-evo- biased populations induced stronger tro- habitat use. Results showed that

lutionary perspective, is at the population phic cascades, causing changes even to female-biased populations spent more

level. ecosystem properties such as water tem- time in the benthic zone and grazed down

perature and pH. When comparing the benthic prey relative to pelagic prey, thus

Populations Link Dimorphism Evo effect size of sex ratio (female-biased vs. inducing a community shift towards the

to Eco male-biased) to the effect size of mosquito- dominance of pelagic prey. These results

To date, effects of sexual dimorphism fish presence versus absence, sex ratio highlight that, even in cases of inconspic-

have been studied experimentally at the effects were up to approximately half as uous morphological dimorphism, ecologi-

population level through the manipulation strong as the effects of mosquitofish pres- cal effects of sexual dimorphism can still

of population sex ratios. This approach ence itself. Thus, the strong and diverse be significant.

2 Trends in Ecology & Evolution, Month Year, Vol. xx, No. yy

TREE 2534 No. of Pages 4

(A) (B) (C) (D)

(E) (F)

Figure 2. Taxa Described in the Main Text. Some of these taxa have hypothesized community and ecosystem effects of sexual dimorphism, (A) huia (Heteralocha

acutirostris) and (B) mosquitoes (e.g., Ochlerotatus sp., pictured), whereas others from recent experiments show significant effects of sexual dimorphism, (C) mulefat

(Baccharis salicifolia), a dioecious shrub from the American southwest; (D) a dioecious shrub from Japan (Eurya emarginata); (E) mosquitofish (Gambusia affinis); and (F)

eastern North American newt (Notophthalmus viridescens). Some species show stark morphological dimorphism, while others show more cryptic dimorphism, for

example, in traits such as nectar concentration (D) and habitat use (F). Females are pictured on the right, and males are pictured on the left in each instance.

Photographs reproduced from K. Mooney (C), K. Tsuji (D), and D. Weiler (E).

Towards Sexual Dimorphism in sexual dimorphism remains a challenge. evolutionary dynamics. Moreover, sex

an Eco-Evo Framework In particular, sex ratio manipulations mod- ratio manipulations confound dimor-

Sex ratio manipulations are useful as ify trait distributions in ways that are not phism-shaped trait distributions with

approaches to understanding the effects evolved and, relatedly, they do not test behaviors associated with ongoing sexual

of existing sexual dimorphism, but con- how contemporary evolution of sexual selection (e.g., male harassment of

necting results to ongoing evolution of dimorphism operates to influence eco- females increases with increasing male-

Trends in Ecology & Evolution, Month Year, Vol. xx, No. yy 3

TREE 2534 No. of Pages 4

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© 2019 Elsevier Ltd. All rights reserved.

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4 Trends in Ecology & Evolution, Month Year, Vol. xx, No. yy